524
erosion) that negatively impacts the resilience of organisms/populations (Bijlsma
and Loeschcke 2011). The magnitude of diversity loss caused by a bottleneck is not
only related to N E but also to the length of time in generations that populations
persist at small N E and the amount of gene flow between populations (Nei et al.
1975). Exposure to contaminants can negatively affect connectivity (Puritz and
Toonen 2011) causing a feedback loop between decreasing population size,
decreasing connectivity (gene flow), and decreasing fitness that can lead to rapid
extirpation (Frankham et al. 2014). This means that populations that are small and
isolated to begin with are at greater risk of genetic erosion following an acute oil
exposure. Direct assessment of horsefly populations following the DWH oil spill
suggests that such a dynamic might be occurring; populations in heavily oiled habitat showed evidence of bottlenecks, reduced migrant rates, and reductions in the
number of individuals (Husseneder et al. 2016). For red snapper and golden tilefish,
evidence for decreased genome-wide variation is lacking, but shifts in allele frequencies at specific loci in areas impacted by oil have been observed (O’Leary pers.
comm.). Because these species have long generation times and high potential connectivity, drift is expected to be weak, suggesting that observed changes in allele
frequencies at specific loci may reflect losses of diversity caused by non-representative gamete sampling, resulting from high mortality and/or intense selection
(Schiebelhut et al. 2018).
Prolonged selection pressure caused by human activities can lead to rapid phenotypic and underlying genetic change in wild populations, a phenomenon sometimes referred to as anthropogenic evolution (Palumbi 2001). Common examples
of anthropogenic evolution often involve “resistance phenotypes” that evolve in
response to toxin exposure; examples include plant resistance to heavy metals
(Antonovics et al. 1971), microbial resistance to antibiotics (Andersson and
Hughes 2010), and insect resistance to pesticides (Whalon et al. 2008). Because
individual organisms have a range of tolerance to oil exposure, related to genetically determined phenotypes, both acute and chronic exposure can cause directional selection favoring resistance to oil-based contaminants. Phase I reactions of
the AHR pathway, the first step in the xenobiotic metabolism of PAHs, may bioactivate or increase the toxicity of compounds (Denison and Nagy 2003; Harrigan
et al. 2004; Shimada 2006; Shiizaki et al. 2017). Thus, activation of the AHR pathway itself presents a challenge to organisms, and prolonged activation can be a
selective agent (Whitehead et al. 2017). Fishes living in environments heavily and/
or chronically contaminated with industrial toxins show heritable resistance to levels of contaminants that are normally lethal and an associated repression of the
AHR pathway (Wirgin et al. 2011; Oziolor et al. 2014; Di Giulio and Clark 2015).
When analyzed at the nucleotide level, patterns consistent with strong, directional
selection have been detected in specific regions of the genomes associated with the
AHR pathway in killifish (Whitehead et al. 2012b; Nacci et al. 2016). Because of
the polygenic nature of resistance, tolerant populations of killifish show distinctive
D. S. Portnoy et al.
erosion) that negatively impacts the resilience of organisms/populations (Bijlsma
and Loeschcke 2011). The magnitude of diversity loss caused by a bottleneck is not
only related to N E but also to the length of time in generations that populations
persist at small N E and the amount of gene flow between populations (Nei et al.
1975). Exposure to contaminants can negatively affect connectivity (Puritz and
Toonen 2011) causing a feedback loop between decreasing population size,
decreasing connectivity (gene flow), and decreasing fitness that can lead to rapid
extirpation (Frankham et al. 2014). This means that populations that are small and
isolated to begin with are at greater risk of genetic erosion following an acute oil
exposure. Direct assessment of horsefly populations following the DWH oil spill
suggests that such a dynamic might be occurring; populations in heavily oiled habitat showed evidence of bottlenecks, reduced migrant rates, and reductions in the
number of individuals (Husseneder et al. 2016). For red snapper and golden tilefish,
evidence for decreased genome-wide variation is lacking, but shifts in allele frequencies at specific loci in areas impacted by oil have been observed (O’Leary pers.
comm.). Because these species have long generation times and high potential connectivity, drift is expected to be weak, suggesting that observed changes in allele
frequencies at specific loci may reflect losses of diversity caused by non-representative gamete sampling, resulting from high mortality and/or intense selection
(Schiebelhut et al. 2018).
Prolonged selection pressure caused by human activities can lead to rapid phenotypic and underlying genetic change in wild populations, a phenomenon sometimes referred to as anthropogenic evolution (Palumbi 2001). Common examples
of anthropogenic evolution often involve “resistance phenotypes” that evolve in
response to toxin exposure; examples include plant resistance to heavy metals
(Antonovics et al. 1971), microbial resistance to antibiotics (Andersson and
Hughes 2010), and insect resistance to pesticides (Whalon et al. 2008). Because
individual organisms have a range of tolerance to oil exposure, related to genetically determined phenotypes, both acute and chronic exposure can cause directional selection favoring resistance to oil-based contaminants. Phase I reactions of
the AHR pathway, the first step in the xenobiotic metabolism of PAHs, may bioactivate or increase the toxicity of compounds (Denison and Nagy 2003; Harrigan
et al. 2004; Shimada 2006; Shiizaki et al. 2017). Thus, activation of the AHR pathway itself presents a challenge to organisms, and prolonged activation can be a
selective agent (Whitehead et al. 2017). Fishes living in environments heavily and/
or chronically contaminated with industrial toxins show heritable resistance to levels of contaminants that are normally lethal and an associated repression of the
AHR pathway (Wirgin et al. 2011; Oziolor et al. 2014; Di Giulio and Clark 2015).
When analyzed at the nucleotide level, patterns consistent with strong, directional
selection have been detected in specific regions of the genomes associated with the
AHR pathway in killifish (Whitehead et al. 2012b; Nacci et al. 2016). Because of
the polygenic nature of resistance, tolerant populations of killifish show distinctive
D. S. Portnoy et al.